Modulation of cortical beta oscillations influences motor vigor: A rhythmic TMS-EEG study

Abstract

Previous electro- or magnetoencephalography (Electro/Magneto EncephaloGraphic; E/MEG) studies using a correlative approach have shown that β (13-30 Hz) oscillations emerging in the primary motor cortex (M1) are implicated in regulating motor response vigor and associated with an anti-kinetic role, that is, slowness of movement. However, the functional role of M1 β oscillations in regulation of motor responses remains unclear. To address this gap, we combined EEG with rhythmic TMS (rhTMS) delivered to M1 at the β (20 Hz) frequency shortly before subjects performed an isometric ramp-and-hold finger force production task at three force levels. rhTMS is a novel approach that can modulate rhythmic patterns of neural activity. β-rhTMS over M1 induced a modulation of neural oscillations to β frequency in the sensorimotor area and reduced peak force rate during the ramp-up period relative to sham and catch trials. Interestingly, this rhTMS effect occurred only in the large force production condition. To distinguish whether the effects of rhTMS on EEG and behavior stemmed from phase-resetting by each magnetic pulse or neural entrainment by the periodicity of rhTMS, we performed a control experiment using arrhythmic TMS (arTMS). arTMS did not induce changes in EEG oscillations nor peak force rate during the rump-up period. Our results provide novel evidence that β neural oscillations emerging the sensorimotor area influence the regulation of motor response vigor. Furthermore, our findings further demonstrate that rhTMS is a promising tool for tuning neural oscillations to the target frequency.

Keywords: cortical oscillations; motor control; primary motor cortex.

FIGURE 1

Trial structure and force production task. (a) Subjects were instructed to perform a visually‐guided force production task to match one of three different targets (5%, 10%, and 25% of MVC) by pressing a force–torque transducer with their right index fingertip. After 2 s from the visual “Rest” cue, the target force level was displayed on the monitor (i.e., “Ready” cue). Rhythmic TMS (rhTMS) and arrhythmic TMS (arTMS) for Experiment 1 and 2 were applied over left M1 through short burst of 5 pulses in a subset of trials 300 ms prior to visual “Go” cue (sky‐blue horizontal line). After receiving the visual “Go” cue, subjects were asked to press on the force sensor with their index fingertip for 3 s throughout the “Keep force level” cue at the required force level as quickly and accurately possible. After receiving the visual “End” cue, subjects were asked to release the index fingertip from the force sensor and relax their right hand. (b) Stimulus pattens of rhTMS and arTMS. In rhTMS, five consecutive magnetic pulses were applied at 20 and 40 Hz. In arTMS, the timing of 2nd to 4th magnetic pulses were randomly jittered with an across‐trial mean frequency of either 20 or 40 Hz depending on the stimulation condition. (c) Subject's hand posture during the data collection and a device instrumented with force/torque sensor. This sensor detects the load along Z‐axis. (d) Typical force time course and trial events: “Ready” cue, rhTMS onset, and “Go” cue

FIGURE 2

Peak force rate. Group‐averaged peak force rate for each target force and trial type for the β‐ and low γ‐rhTMS groups (a and b, respectively). Boxplots depict median (crossbar) and minimum and maximum values (whiskers). Open circles denote outlier. Statistically significant differences were determined using a liner‐mixed model. *** denote statistically significant differences at p < .001.

FIGURE 3

Effect of β‐rhTMS on zPLF in β frequency. (a) Group‐averaged time‐frequency representation of zPLF across significant EEG channels identified at the 25% MVC condition. Green dotted lines denote the frequency band and time window used for averaging zPLF values for each force condition. (b) Topographical plots of group‐averaged zPLF in the β‐frequency band. Based on cluster‐based comparisons, t statistical map was shown at the right column using red‐blue scale and significant channels between β‐rhTMS and sham are overlaid as red dots (cluster‐threshold: p < .05). Higher synchronous EEG oscillations in the β‐frequency band were distributed across the contra‐ and ipsilateral sensorimotor areas and especially for the 25% MVC condition (bottom row).

FIGURE 4

Effect of γ‐rhTMS on zPLF on γ‐frequency. (a) Group‐averaged time‐frequency representation of zPLF at C3 channel in the 25% MVC condition. Dot lines denote the frequency band and time window used for averaging zPLF values were averaged for each force condition. (b) Topographical plots of group‐averaged zPLF in the γ‐frequency band (38–45 Hz). Based on cluster‐based comparisons, t statistical map was shown at the right column using red‐blue scale and significant channels between γ‐rhTMS and sham are overlaid as red dots (cluster‐threshold: p < .05). Lower synchronous EEG oscillations in the γ‐frequency band were identified in the 25% MVC than sham condition (b, bottom row).

FIGURE 5

Baseline EEG power changes (catch trial) in each force level. (a) Topographical plots of group‐averaged EEG power in the β‐frequency band (−300 to −50 ms relative to “Go cue”: Same time window as rhTMS) that were obtained from the catch trials. (b) Whole channel averaged EEG powers in the β frequency band across the force level. *** and † depict p < .001 and .07, respectively.

FIGURE 6

EEG and behavioral results of the arTMS condition. (a) Effects of arTMS on the zPLF changes. Using cluster‐based comparisons, statistical t‐map is illustrated at the middle of this figure. (b) Effects of arTMS on peak force rate. Boxplots depict median (crossbar) and minimum and maximum values (whiskers). Boxplots visualizing group‐averaged peak force rate in each condition. The mixed effect linear model yielded no significant differences in peak force rate across the stimulus condition within the both MVC condition.